Invasive alien plants in China: role of clonality and geographical origin

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1 Biological Invasions (2006) 8: Ó Springer 2006 DOI /s x Invasive alien plants in China: role of clonality and geographical origin Jian Liu 1,2, Ming Dong 1,2,6, *, Shi Li Miao 3, ZhenYu Li 4, Ming Hua Song 5 & Ren Qing Wang 2 1 Key Laboratory of Quantitative Vegetation Ecology, Institute of Botany, the Chinese Academy of Sciences, Beijing, , P. R. China; 2 School of Life Sciences, Shandong University, Ji nan, , P. R. China; 3 Everglades Division, South Florida Water Management District, 3301 Gun Club Road, West Palm Beach, FL, 33406, USA; 4 Laboratory of Systematic and Evolutionary Botany, Institute of Botany, the Chinese Academy of Sciences, Beijing, , P. R. China; 5 Institute of Geographical Sciences and Natural Resources Research, the Chinese Academy of Sciences, Beijing, , P. R. China; 6 Institute of Botany The Chinese Academy of Sciences, Beijing, , P. R. China; *Author for correspondence ( dongming@ibcas.ac.cn; fax: ) Key words: China, clonality, geographic origin, plant invasions, plant traits Abstract Biological invasions have become a significant threat to the global environment. Unfortunately, to date there is no consensus on invasion mechanisms and predictive models. Controversies range from whether we can reliably predict which species may become invasive to which species characteristics (e.g., life history, taxonomic groups, or geographic origin) contribute to the invasion processes. We examined 126 invasive alien plant species in China to understand the role of clonality and geographical origin in their invasion success. These species were categorized into three groups (I, II, III) based on their invasiveness in terms of current spatial occupation and the degree of damage to invaded habitats. Clonal plants consisted of almost half (44%) of the 126 invasive species studied, and consisted of 66% of 32 the most invasive alien plant species (Group I). There was a significant positive relationship between clonality and species invasiveness. A 68% of the 126 species studied originated in the continent of America (North and/or South America). These preliminary findings support that America is the primary geographical origin of invasive alien plant species in China and that clonality of the invasive plant species contributed significantly to the their invasiveness. The results suggest an urgent need at the global scale to investigate the mechanisms whereby plant clonal growth influences plant invasions, and the need for a focus at regional scale to examine factors affecting the exchange of invasive plant species between America and China. Introduction Plant invasion has become a significant threat to biodiversity, environment and economies both globally and locally (Mack et al. 2000; Pimentel et al. 2000; Liu et al. 2001; Mitchell and Power 2003). It is critical to analyze the invasive ability of alien plants before introduction so that likely invasive species can be screened (Goodwin et al. 1999). Thus, two of the urgent tasks of ecologists who are investigating biological invasions are to understand the factors influencing invasion success of plants and to develop means to predict plant invasions (Heger and Trepl 2003). Unfortunately, to date there is no consensus on invasion mechanisms and predictive models (Alpert et al. 2000; Milbau

2 1462 et al. 2003). Controversies range from whether we can reliably predict which species may become invasive to which species characteristics (e.g., life history, taxonomic groups, or geographic origin) contribute to the invasion processes. Clonality, an important trait enhancing plants exploitation of ubiquitous environmental heterogeneity, may aid plants to invade new habitats (Maurer and Zedler 2002). Also, clonality can contribute to spatial occupation at a local scale and risk spreading of the clonal plants (Dong 1996b). Asexual clonal reproduction is one of the characters of some highly invasive plants (Baker 1974; Sakai et al. 2001). A considerable number of invasive plant species have the capability of vigorous clonal propagation and their invasiveness maybe related to clonality (Leakey 1981; Dong 1996a; Rejma nek 1999; Kolar and Lodge 2001). Yet, we found few studies to support this conclusion quantitatively. The geographical origin of alien species may influence their invasiveness in new areas (Reichard 2001; Lloret et al. 2004). In addition, species from a large continent may more easily invade a new habitat where the climate is similar to their geographical origin, as compared to species from a small continent and in new habitat having a different climate (Mihulka and Pysˇ ek 2001). Successful invaders mainly originate from large continents with diverse biota (Sax and Brown 2000). China is the third largest country in the world in terms of territory and possesses mega-diversity of plant species with numerous invasive alien plant species (Xie et al. 2000). However, there are a few quantitative analysis of geographic origin for invasive species in China. In this study, we analyzed characters of 126 major invasive alien plant species in China, including plant traits such as clonality, life form, and geographic origin to understand the role of clonality and geographical origin in their invasion success. Methods Data collection So far, a few researchers have published different lists of invasive alien plants existing in China. For instance, 58, 90 and 80 invasive alien plant species were reported by Ding and Wang (1998), Li and Xie (2002) and Xiang et al. (2002), respectively. We integrated the data from those three lists according to the definition of invasive plants by Richardson et al. (2000) and Pysˇ ek et al. (2004), i.e., invasive plants are a subset of naturalized plants that produce reproductive offspring, often in very large numbers, at considerable distances from the parent plants, and thus have the potential to spread over a large area. We removed the overlapping species and corrected wrong records. As a result, a new list containing 126 major invasive plant species was derived and used for the present study. We extensively consulted published literature for the data of each of the species (Editorial Board for Flora of China ; Li 1998; Li and Xie 2002). Data from literature were used to construct a detailed database for the plant species under study, including characters such as invasiveness, plant traits, provincial distribution and geographic origin. The geographic origin in our study refers to evolutionary origin where the plant species evolved as a native species. Data analyses A geographic distribution map, based on the number of invasive plant species, was made according to the distribution information listed in our detailed database using Arcview GIS 3.2. Plant traits that can be identified and used easily were chosen (Reichard 2001). The traits selected in this study were clonality, life form, geographical origins, provincial distribution and invasiveness. Based on clonality, the plants were divided into clonal plants, with different types of clonal organs and non-clonal plants; while based on life form, the plants were categorized as annual and perennial herbs and shrubs. The geographical origins included America, Europe, Africa and Asia. In general it is difficult to determine the invasiveness of a species, however we evaluated plants invasiveness in terms of their current spatial occupation and impacts that can be obtained from literature. The 126 species were divided into three groups. The invasiveness decreases from group I, group II to group III. The first group (Group I) consists of

3 1463 those species that occupied extensive areas and/or with severe damage to local diversity. These species have all been listed in the books 100 of the World s Worst Invasive Alien Species (IUCN 2001) and/or The World s Worst Weeds (Holm et al. 1977), except for Eupatorium adenophorum and Alternanthera philoxeroides, which have been recorded recently as notorious invasive alien plants in China (Li and Xie 2002). The second group (Group II) includes those species that occupied large area (>300 km 2 ) and/or had strong negative influence. The third group (Group III) contains those species that occupied a relatively small area and/or had relatively small harmful impacts. According to the habitats the plants invaded, the 126 invasive alien plant species in China were also divided into the following categories: natural area invaders inhabiting areas experiencing slight human disturbance (e.g. forest and wetland); non-natural area invaders inhabiting areas experiencing strong human disturbance (e.g. roadside and cropfield); and invaders of both areas (Daehler 1998; Li 1998; Li and Xie 2002). Spearman s correlations were made for all the characters using SPSS (SPSS for Windows, Rel , 1999, Standard Version). Results Clonality and invasiveness Based on Ding and Wang (1998), Li and Xie (2002) and Xiang et al. (2002), a total of 126 major alien invasive species in China was studied for their clonality, life form, geographic origin and invasiveness (Appendix A). The number of invasive plant species decreases towards more western and northern China (Figure 1). Over 60% of these species invaded non-natural areas (Figure 2). These species showed different degrees of invasion success at the time of the investigation. Approximately 25% of the 126 species were the Figure 1. The provincial distribution of the 126 invasive alien plant species in China. The species richness of invasive plants in every provincial administrative unit was collected according to the distribution information. Arcview GIS 3.2 was used for the figure of the distribution pattern. The color codes represent the number of species in each province.

4 1464 Number of species All plants Clonal plants Non-natural area Natural area Both areas Habitats Figure 2. The number of clonal plants found in different habitats including natural areas (forests and wetlands with relatively low human disturbance), non-natural area (crop-lands and roadsides with relatively high human disturbance), and both natural and non natural areas. most invasive species (Group I); 31% were those with invaded area >300 km 2 (Group II) exhibiting strong negative influence in the invaded area; and 43% made as the third group (Group III) containing species that occupied relatively small area and/or had relatively small harmful impact. Clonal plants consist of almost half (44%) of the 126 species, including 17% with rhizomes, 11% with stolons, 11% with tillers and 14% with other clonal organs (e.g. tubers and/or bulbs) (Table 1). Some clonal plants had more than one type of clonal organ. For example, Alternanthera philoxeroides uses stolons and storage roots and Cyperus rotundus uses rhizome and tubers for propagation. Clonal plants accounted for 66% of 32 most invasive species (Group I). A significant positive correlation between clonality and invasiveness (P<0.05, based on the 126 species) was identified by the Spearman s correlation analyses (Table 2). In particular, clonal species with stolon and tiller showed significant correlations with invasiveness. While only 28% of the clonal plants were found in the non-natural area invaders, 56% were found in the natural areas and 64% were found in both areas (Figure 2). Plant life form and invasiveness Herbaceous species (both perennial and annual) accounted for 88% of the 126 alien invasive species, whereas shrub species was about 11% Table 1. Analyses of the degree of invasiveness and clonality of 126 invasive alien plant species in China. Invasiveness Total # Clonal plants Total # No. of species with rhizome No. of species with stolons No. of species with tillers No. of species with other types of clonal organs Group I Group II Group III Total Note: A plant species can have multiple clonal organs.

5 1465 Table 2. Summary of Spearman s correlation analyses based on clonality and life form for 126 invasive alien plant species in China. r Invasiveness Clonality Clonal organs Life forms Rhizome Stolon Tiller Other Annual Perennial Invasiveness Clonality 0.28* Clonal organs Rhizome 0.07 ns 0.51* Stolon 0.24* 0.40* )0.16 ns Tiller 0.25* 0.40* 0.17 ns )0.12 ns Others )0.05 ns 0.46* 0.06 ns 0.14 ns )0.14 ns Life forms Annual 0.07 ns )0.23 ns )0.15 ns )0.11 ns )0.01 ns )0.22* Perennial )0.05 ns 0.28* 0.22* 0.19* 0.09 ns 0.14 ns )0.79* Shrub )0.03 ns )0.08 ns )0.10 ns )0.13 ns )0.13 ns 0.13 ns )0.32* )0.33* *=P<0.05; ns=not significant. (Table 3). Although perennial and annual herbs showed a similar ratio, among the 126 species, 45% and 42%, respectively, the former had 2 times more clonal plants than the latter (60% vs. 31%) (Table 3). Geographic origin of the invasive species As high as 68% of the 126 invasive plants species originated in America (North/South) (Table 4). Species with European origin accounted only 18% and Africans and Asian origin was the lowest, 3%. Similarly, species with American origination contributed the highest percentage (22 out of 32 species) for the most invasive species group (Group I). American origin species showed the highest percent (25) of clonal plants, whereas only 10%, 5% and 4% clonal plants were from Europe, Africa and Asia, respectively (Figure 3). Discussions Our analyses showed that clonality might play an important role in the invasion process and success for alien species studied in China. Almost half of the species studied and over 60% of the most invasive species (Group I) are clonal plants. Moreover, there was a significantly positive correlation between clonality and the invasiveness. These findings provide new evidence linking clonality to plant invasion, which is in accordance with previous studies based on individual species. For example, Pysˇ ek et al. (2003) found that novel hybrid invasive genotypes may be produced by rare sexual reproduction, fixed by clonal growth, and presents a previously unknown threat to native vegetation. Maurer and Zedler (2002) suggested that both the resource subsidy from parent clones and resource foraging plasticity contribute to invader s ability to spread rapidly into native vegetation. Reichard and Hamilton (1997) studied the invasive plants of America and also found that clonality may enhance invasion. However, the field study of Populus tremuloides by Peltzer (2002) showed that clonal integration tended to improve ramet survival and growth, but these trends were often not significant in the species. The relationship between Table 3. Analyses of invasive alien plant species with different life forms in China. Life form Total # Clonal plants Total # Rhizome Stolon Tiller Others Annual Perennial Shrub Note: A plant species can have multiple clonal organ.

6 1466 Table 4. Analyses of geographic origins of 126 invasive alien plant species in China. Invasiveness America Europe Africa Asia Group I Group II Group III Total clonality and invasiveness in plants may be species specific. Plants with high invasiveness are often very adaptive. They may displace the native species through competition (Chittka and Schurkens 2001). Clonal plants are regarded as being especially adaptive in heterogeneous environments and contribute greatly in most ecosystems (Hutchings and de Kroon 1994; Dong 1996a; Song et al. 2002). Their adaptive advantages are mainly due to their genetic risk spreading via cloning (Cook 1985; Dong 1996b), intraclonal sharing of resources (Peltzer 2002), foraging behavior (Hutchings and de Kroon 1994; Dong 1996a) and division of labor in clone (Alpert and Stuefer 1997) in spatially heterogeneous (patchy) habitats. Compared to non-clonals, clonal invaders appear to suffer a disadvantage in the dispersal phase of invasion because ramets are usually not able to disperse to great distance (Pysˇ ek 1997). However, most clonal plants possess both asexual (clonal) propagation and sexual reproduction (Eckert 2002) and allocation to both modes may be plastic. For instance, several notorious plant invaders, such as Mikania micrantha, Eupatorium adenophorum, combine sexual reproduction with strong clonal propagation, (Huang et al. 2000; Song and Dong 2002). The present study also suggested that America was the primary geographical origin of most invasive alien plant species in China. Asia and North America share a wide range of similar environments and related biota, which may result in each region being more susceptible to each other s immigrant species than species from many other parts of the world (Guo 1999, 2002). Moreover, exchanges of alien plants and animals across the Pacific Ocean are increasing markedly as commerce between these two regions has soared in the past few decades; the rate of these species exchanges will undoubtedly accelerate. Thus, there is an urgent need at the global scale to investigate the mechanisms whereby plant clonal growth influences plant invasions, and the need to focus at regional scale to examine factors affecting the exchange of invasive plant species between America and China. 30 Percentageof clonal plants (%) America Europe Africa Asia Geographic origins Figure 3. Percentage of clonal plant species based on geographic origins for the 126 invasive alien plant species in China.

7 1467 Our results revealed a trend of provincial distribution of invasive alien plant species in China that the number got less towards more western and northern places. This illustrates widely the occurrence of invasive alien plants in China and implicates a correlation of plant invasion to the degree of development of economy and society because in general the degree is higher, in addition to national conditions is more favorable for plants, in more eastern and southern places in China. Acknowledgements We thank anonymous referees for their valuable comments on the manuscript. The article was supported financially by National Science Fund for Distinguished Youth Scholars of China (No ) for M.D., Oversea Distinguished Scholar of CAS for S.L.M. and Key Project of Natural Science Foundation of Shandong Province (No. Z2003 D05). Appendix A Table A1. Checklist of 126 invasive plants in P.R. China and their clonality, life forms, geographic origins, and invasiveness. Species Clonality Life forms Geographic origins Invasiveness Acacia farnesiana No Shrub America Group III Acanthospermum australe No Annual America Group III Ageratum conyzoides No Annual America Group I Agrostemma githago No Annual Europe Group II Alternanthera philoxeroides Yes Perennial America Group I Alternanthera pungens Yes Annual America Group II Amaranthus albus No Annual America Group II Amaranthus chlorostachys No Annual America Group III Amaranthus polygonoides No Annual America Group II Amaranthus retroflexus No Annual America Group II Amaranthus spinosus No Annual America Group I Amaranthus viridis No Annual Africa Group II Ambrosia artemisiifolia No Annual America Group II Ambrosia trifida No Annual America Group III Anredera cordifolia Yes Perennial America Group II Apium leptophyllum No Annual America Group III Aster subulatus Yes Annual America Group II Avena fatua Yes Annual Europe Group I Axonopus compressus Yes Perennial America Group I Bidens frondosa No Annual America Group III Bidens pilosa No Annual America Group I Cabomba caroliniana Yes Perennial America Group II Cenchrus echinatus Yes Annual America Group I Chenopodium ambrosioides No Perennial America Group II Chenopodium hybridum No Annual Europe Group II Conyza bonarinisis No Annual Europe Group III Conyza canadensis No Annual America Group II Conyza sumatrensis No Perennial America Group III Coreopsis tinctoria No Annual America Group III Coronopus didymus No Perennial America Group II Crassocephalum crepidioides No Annual Africa Group II Cyperus rotundus Yes Perennial Asia Group I Datura stramonium No Annual America Group II Daucus carota No Perennial Asia Group III Eichhornia crassipes Yes Perennial America Group I Eleusine indica Yes Annual Asia Group I

8 1468 Table A1. Continued. Species Clonality Life forms Geographic origins Invasiveness Erigeron annuus Yes Annual America Group I Erigeron philadelphicus No Perennial America Group III Eryngium foetidum No Perennial America Group III Eupatorium adenophorum Yes Shrub America Group I Eupatorium catarium No Annual America Group II Eupatorium odoratum Yes Perennial America Group I Euphorbia dentata No Annual America Group III Euphorbia helioscopia No Perennial America Group II Euphorbia hirta No Annual Africa Group I Euphorbia maculata Yes Annual America Group II Galinsoga parviflora No Annual America Group I Geranium carolinianum No Perennial America Group III Gomphrena celosioides No Annual America Group III Helenium autumnale No Perennial America Group III Heliotropium europaeum No Annual Europe Group III Hibiscus trionum No Annual Africa Group II Hyptis rhomboidea No Annual America Group III Hyptis suaveolens No Annual America Group III Ipomoea cairica Yes Perennial America Group III Ipomoea purpurea No Perennial America Group II Lantana camara No Shrub America Group I Lemna trinervis Yes Perennial America Group II Lepidium campestre No Perennial Europe Group III Lepidium perfoliatum No Perennial Europe Group III Lepidium virginicum No Perennial America Group II Leucaena leucocephala No Shrub America Group I Lolium multiflorum Yes Annual Europe Group II Lolium temulentum Yes Annual Europe Group I Macfadyena unguis-cati Yes Shrub America Group III Malvastrum coromandelianum Yes Perennial America Group III Melilotus albus No Perennial Europe Group II Mikania micrantha Yes Perennial America Group I Mimosa invisa No Shrub America Group I Mimosa invisa var.inermis No Shrub Asia Group III Mimosa pudica No Shrub America Group I Mirabilis jalapa Yes Annual Africa Group II Nasturtium officinale Yes Perennial Europe Group II Oenothera rosea No Perennial America Group III Opuntia ficus-indica Yes Shrub America Group III Opuntia monacantha Yes Shrub America Group III Opuntia stricta var.dillenii Yes Shrub America Group III Oxalis corymbosa Yes Perennial America Group II Panicum maximum Yes Perennial Africa Group I Panicum repens Yes Perennial America Group I Papaver nudicaule Yes Perennial Europe Group III Parthenium hysterophorus No Annual America Group III Paspalum conjugatum Yes Perennial America Group I Paspalum dilatatum Yes Perennial America Group I Passiflora foetida No Perennial America Group III Peperomia pellucida Yes Annual America Group II Pharbitis nil No Annual America Group III Phleum pratense Yes Perennial Europe Group III Physalis pubescens No Perennial America Group III Phytolacca americana No Perennial America Group II Pilea microphylla No Annual America Group III

9 1469 Table A1. Continued. Species Clonality Life forms Geographic origins Invasiveness Pistia stratiotes Yes Annual America Group I Plantago virginica Yes Annual America Group II Polymnia uvedalia No Perennial America Group III Rhynchelytrum repens Yes Perennial Africa Group III Ricinus communis Yes Annual Africa Group III Scoparia dulcis No Annual America Group III Senecio dubtabilis Yes Annual Europe Group III Senecio vulgaris Yes Annual Europe Group II Setaria palmifolia Yes Perennial Africa Group III Solanum aculeatissimum No Annual America Group III Solanum capsicoides No Perennial America Group II Solanum erianthum No Shrub America Group III Solanum torvum No Shrub America Group III Solidago canadensis Yes Perennial America Group III Soliva anthemifolia No Perennial America Group III Sorghum halepense Yes Perennial Europe Group I Spartina alterniflora Yes Perennial America Group II Spartina anglica Yes Perennial Europe Group I Spergula arvensis Yes Annual Europe Group I Spermacoce latifolia No Perennial America Group III Stachytarpheta jamaicensis No Shrub America Group III Stellaria apetala No Perennial Europe Group III Synedrella nodiflora No Annual America Group III Tridax procumbens Yes Perennial America Group II Trifolum repens Yes Perennial Europe Group III Ulex europaeus No Shrub Europe Group I Vaccaria segetalis No Annual Europe Group II Veronica hederifolia Yes Perennial Europe Group III Veronica persica Yes Perennial Asia Group II Veronica polita Yes Perennial Asia Group II Vetiver zizanioides Yes Perennial Asia Group II Waltheria indica Yes Perennial America Group III Wedelia chinensis Yes Perennial Africa Group III Wedelia trilobata Yes Perennial America Group I Xanthium spinosum No Annual America Group I References Alpert P and Stuefer JF (1997) Division of labour in clonal plants. In: de Kroon H and van Groenendael J (eds) The Ecology and Evolution of Clonal Plants, pp Backhuys Publishers, Leiden Alpert P, Bone E and Holzapfel C (2000) Invasiveness, invasibility, and the role of environmental stress in preventing the spread of non-native plants. Perspectives in Plant Ecology, Evolution and Systematics 3: Baker HG (1974) The evolution of weeds. Annual Review of Ecology and Systematics 5: 1 24 Chittka L and Schurkens S (2001) Successful invasion of a floral market. Nature 411: 653 Cook RE (1985) Growth and development in clonal plant population. In: Jackson JBC, Buss LW and Cook RE (eds) Population Biology and Evolution of Clonal Organism, pp Yale University Press, New Haven Daehler CC (1998) The taxonomic distribution of invasive plants: ecological insights and comparison to agricultural weeds. Biological Conservation 84: Ding JQ and Wang R (1998) Invasive alien plant species and their impact on biodiversity in China. In: Compilation Group of China s Biodiversity (eds) China s Biodiversity: A Country Study, pp China Environmental Science Press, Beijing Dong M (1996a) Clonal growth in plants in relation to resource heterogeneity: foraging behavior. Acta Botanica Sinica 38: Dong M (1996b) Plant clonal growth in heterogeneous habitats: risk-spreading. Acta Phytoecologica Sinica 20: Eckert CG (2002) The loss of sex in clonal plants. Evolutionary Ecology 15: Editorial Board for Flora of China ( ) Flora of China. Science Press, Beijing

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